animals

Review
Defining “Normal” in Pig Parturition
Alexandra Walls 1 , Bianca Hatze 1 , Sabrina Lomax 2 and Roslyn Bathgate 1, *

1 Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Sydney 2006, Australia
2 School of Life and Environmental Sciences, Faculty of Science, The University of Sydney,
Sydney 2006, Australia
* Correspondence: [email protected]

Simple Summary: The dual considerations of efficient food production and good animal welfare have
never been so important nor under such strong public scrutiny as they are in current times. Intensive
animal production industries play an important role in feeding an ever-growing, increasingly affluent
population that is hungry for animal proteins. The efforts to improve efficiency in these production
systems must not come at the cost of animal welfare. One pain point in pig production is that of
parturition, where factors such as litter size and sow-housing type have been shown to influence
the process and outcome. However, there are still many gaps in knowledge surrounding the normal
physiology and endocrinology in a farrowing and this review seeks to summarise what is known and
highlight areas where further work is required.

Abstract: Animal production industries rely on efficient and successful reproductive outcomes, with
pigs being no exception. The process of parturition in pigs (farrowing) can be especially prolonged,
due to the large numbers of piglets being born (on average, approximately 13 piglets per litter in
Australian conditions). Difficulties in farrowing (dystocia) lead to poor piglet outcomes and health
problems in sows, in turn, causing economic loss for producers and welfare concerns for the animals.
Despite the importance of this topic and publications in the area stretching back nearly 50 years, there
is still no consensus on the prevalence of dystocia in pigs nor on how to identify a pig experiencing
Citation: Walls, A.; Hatze, B.; Lomax, the condition. Understanding the process of parturition and the factors that influence its success is a
S.; Bathgate, R. Defining “Normal” in crucial step towards the early identification of sows undergoing dystocia and development of best
Pig Parturition. Animals 2022, 12, practices to assist them. This article describes the key factors that contribute to successful farrowing
2754. https://doi.org/10.3390/ and identifies areas in which more research is required before the parturition process in the pig can
ani12202754
be fully understood.
Academic Editors: Kate J. Plush
and Pieter Langendijk Keywords: behaviour; eutocia; dystocia; reproduction; sow; welfare

Received: 5 September 2022

Accepted: 7 October 2022
Published: 13 October 2022
1. Introduction
Publisher’s Note: MDPI stays neutral
An understanding of mammalian parturition is important for animal production
with regard to jurisdictional claims in
industries as it is one of the keystones for success in this setting, which relies on efficient
published maps and institutional affil-
reproductive outcomes. Although much research has focused on the prevention of problems
iations.
during parturition (dystocia) in ruminants (reviewed by [1,2]), relatively little attention
has been given to the pig in this area. This is perhaps due to the common perception that
the frequency of dystocia in this species is low. Historically, rates of less than 5% have
Copyright: © 2022 by the authors.
been reported [3], but the definition of normal parturition in the pig has not been identified
Licensee MDPI, Basel, Switzerland. adequately and reported ranges of “normal” are widely disparate.
This article is an open access article The limited reports on parturition in the direct ancestors of the domestic pig, the
distributed under the terms and wild pig, suggest that the average litter size is about 6 piglets [4,5] and both the farrowing
conditions of the Creative Commons length and inter-piglet interval vary greatly, but the averages are about 81 min and 26 min,
Attribution (CC BY) license (https:// respectively [5]. Additionally, data from studies in domestic pig parturition from several
creativecommons.org/licenses/by/ decades ago can no longer be relied upon, as they were essentially studying a different
4.0/). animal due to the vast increase in litter sizes and neonatal growth rates resulting from the

Animals 2022, 12, 2754. https://doi.org/10.3390/ani12202754 https://www.mdpi.com/journal/animals

Animals 2022, 12, 2754 2 of 17

genetic selection that led to the development of the modern pig. These modern pigs are
defined by characteristics such as increased growth rates, a leaner carcass, larger litter sizes,
and more stillborns than their counterparts from several decades ago [6–8].
It is clear that periparturient events influence piglet survival [9]. It is also well docu-
mented that difficulties in parturition lead to compromised sow health, with an increased
chance of developing postpartum dysgalactia syndrome (PPDS) observed with the increased
duration of parturition and subsequent decreased chance of successful rebreeding [10]. This,
along with the aim of improving the welfare of the sow in this period, demonstrates the need
to develop an understanding of eutocia in the pig. This review aims to outline the current
understanding of factors that influence parturient success in the pig while highlighting areas
in which there is a knowledge gap requiring further study.

2. The Process of Parturition

Mammalian parturition has been studied most intensively in the human, but the main
concepts can be transferred to most other mammals. The two key events required for a
successful parturition are the opening of the birth canal via softening and dilation of the
cervix (cervical ripening) and the removal of the myometrial blocks to allow for uterine
contractions [11]. Parturition is composed of three stages, the first being the preparatory
stage of cervical ripening and the onset of myometrial contractions to position the first
fetus in the apex of the birth canal. The second stage is defined by the appearance of strong
abdominal contractions, rupture of the allantochorionic sac and expulsion of the fetuses.
The third and final stage includes the expulsion of any remaining fetal membranes (these
are sometimes expelled alongside the fetus in polytocous species) [12].
It is important to note the significant pain associated with this process [12]. Labour
pain is ranked as one of the most intense pains recorded in humans [13]. Based on their
similar anatomy, central nervous system and responses to noxious stimuli, it is reasonable
to assert that other mammals experience pain during parturition [14]. Following this, it
could also be inferred that as in humans, dystocic parturition in pigs causes a significant
amount of pain [12]. This concept is supported by studies showing that sows experience
pain in parturition [15] and is worse in cases of difficult farrowings [14]. Definitions of
normal parturition (eutocia) and dystocia should be established to quantify the impact on
reproductive outcomes on the farm and allow for appropriate intervention such as pain
relief to sows. This will improve welfare and enable better piglet outcomes.

2.1. Pregnancy in the Pig

The length of gestation in the pig is renowned for being “3 months, 3 weeks and
3 days”, but the actual time frame varies between breeds and individuals to be between 105
and 125 days [16]. The fetuses are evenly distributed throughout the bicornate uterus [17],
and placentation is classified as anatomically diffuse and histologically epitheliochorial [18].
The corpora lutea (CL) are present throughout the duration of the pregnancy and remain
the primary source of progesterone throughout this time [19]. The average litter size varies
between breeds, strains and husbandry systems, with examples being 11 in the USA [20] to
nearly 15 in Denmark [21].

2.2. Eutocia and Dystocia

Eutocia in the pig can be defined as the successful expulsion of all fetuses and placentas
without the aid of obstetrical intervention. Dystocia describes a parturient experience that
is slow or difficult, often requiring assistance. Current working definitions of dystocia in
the sow rely heavily on a handful of accounts (summarised in Table 1). Even within the few
publications on this topic, classifications are highly variable, with some suggesting a focus
on inter-piglet intervals [22–25], whereas others suggest a total farrowing duration [26,27]
or a combination of these and other factors. Notably, the figure of a 45–60 min inter-piglet
interval is common across several publications (Table 1), but it is unclear from where this
Animals 2022, 12, 2754 3 of 17

figure is derived. Equally contentious are prevalence rates, which range from 0.25–47% of
spontaneous farrowing [22,27].
Despite the lack of consensus on prevalence, it is agreed that dystocia most commonly oc-
curs in the presence of fetal obstruction or inadequate myometrial contraction activity [3,23].
Obstruction of the fetus within the birthing canal (reported to be responsible for 63% of dys-
tocia cases) [28] can be caused by constipation, mispositioning of the fetus or maternal pelvis
dimensions and, in some cases, a combination of these factors [28]. Inadequate myometrial
contractions at farrowing are reported to be the cause of the remaining cases of dystocia
(37% of cases) [28] and may be caused by fatigue, uterine inertia, hormonal imbalances
and nutritional irregularities [3,23]. With the steady increase in litter size and associated
physiological demands for the sow in modern production systems [6], additional research
is warranted for timely identification and treatment administration to animals in need of
assistance. Notably, further understanding of myometrial activity, appropriate inter-piglet
intervals and behavioural dystocia identifiers are necessary to improve both sow and piglet
welfare [29].

Table 1. Proposed definitions and cited prevalence of dystocia in the pig by previous authors.

Reference Dystocia Classification Prevalence (%)

Inter-piglet interval greater than 45 min,
Nam and Sukon 2021 [30] 47
application of obstetric assistance
Zamemba et al. 2019 [25] Inter-piglet interval greater than 45 min 11.5
Oliviero et al. 2010 [26] A farrowing greater than 300 min N/A
Failure to deliver fetuses within 2 h from
the onset of labour, an inter-piglet interval
Cowart 2007 [23] greater than 1 h, a gestation period beyond 1
116 days, sow illness, discoloured
vulval discharge
Absence of uterine contractions,
Alonso-Spilsbury et al. 2004 [24] inter-piglet intervals greater than 1 h, N/A
application of obstetric assistance
Labour lasting longer than 2 h in duration,
Jones 1966 [27] application of obstetric assistance, 0.25
uterine inertia

3. Endocrinology of Parturition
The details of the key factors that contribute to a successful farrowing in a normal birth
have not been defined in the modern sow. Creating reference ranges for these is important
to differentiate between eutocia and dystocia and will enable an understanding of which
are most significant for piglet survival and sow welfare. There are also external factors that
contribute to the experience of parturition in the pigs, such as the type of housing and diet.
These will also be discussed.

3.1. Periparturient Endocrinology

The endocrine cascade that initiates and controls parturition differs between mam-
malian species, and in several species, begins with the increased secretion of cortisol
from the fetus. In the pig, an increasing concentration of adrenocorticotropic hormone
(ACTH) from the fetal anterior pituitary (adenohypophysis) acts via the fetal hypothalamic–
pituitary–adrenal (HPA) axis to cause secretion of glucocorticoids from the adrenal cortex.
This likely has a significant role in fetal maturation [31], but does not seem to be the ultimate
trigger of parturition in the pig. The increased cortisol redirects endometrium-derived
PGF2α from the uterine lumen, where it is sent under the influence of embryonic oestra-
diol during pregnancy to the uterine vein and, subsequently, into general circulation [32].
This access to the uterine veins gives direct transmission to the ovarian arteries and, thus,
Animals 2022, 12, 2754 4 of 17

initiation of luteolysis. The dominance of luteal-derived progesterone on the maternal

reproductive tract is lost with the onset of luteolysis [31]. Alongside this, the conversion of
any progesterone remaining in the system to oestrogen by the placental-derived enzymes
sees a dramatic switch in the ratio of progesterone: oestrogen. This, in turn, removes
the myometrial block that was imposed by progesterone and initiates contractions under
the influence of oestrogen. These first contractions push the first fetus down onto the
internal os of the cervix and this stimulation creates a positive feedback loop with release
of oxytocin from the posterior lobe of the pituitary (neurohypophysis). Oxytocin stimulates
powerful myometrial contractions, forcing more pressure onto the cervix from the fetus
and, thus, stimulating more oxytocin to be released from the pituitary [33]. Simultaneously,
the increased oestrogen in the system increases mucosal secretion in the reproductive tract,
which creates the lubrication needed for passage of the fetuses. Finally, relaxin secretion
from the CL peaks in the days just prior to parturition, enabling enhanced stretching of
the pelvic ligaments to accommodate the passage of the fetus through the birth canal [34].
The pattern of changing concentrations of these key hormones is summarised in Figure 1.
However, these data should be viewed with the erudite comment of Gilbert, 2001 [35], in
mind; changes of hormone concentration in the circulating blood are not fully informative
without also knowing the relevant receptor expression. This is where there continues to be
a scarcity of data, preventing full understanding of the control of parturition in the pig.

Figure 1. Patterns of periparturient plasma hormone concentrations in the pig. Unscaled. Adapted
from [35] and used with permission.

3.1.1. Oestrogen and Progesterone

Parturition cannot proceed without the removal of the myometrial block imposed
by high concentrations of circulating progesterone during pregnancy [36]. In the pig,
luteolysis (the CL being the main source of progesterone throughout gestation [37]) occurs
about 24 h prior to parturition. With an intravenous half-life of approximately 30 min [38],
the circulating progesterone concentration rapidly declines when it is no longer being
replenished. The corticosteroid parturient trigger stimulates production of oestrogen by
the placenta [39]. This, alongside the cessation of progesterone production due to luteolysis
and the conversion of progesterone to oestrogen by the placentally derived enzymes [40]
over the days prior to parturition, are the drivers behind the dramatic transient rise in
oestrogen that initiates uterine contractions in stage 1 of parturition. These preliminary
contractions assist in positioning the first fetus at the internal os of the cervix, applying
pressure that leads to the release of oxytocin from the posterior lobe of the pituitary gland.
Animals 2022, 12, 2754 5 of 17

Oestrogen also stimulates the formation of oxytocin receptors in the uterus [41] that work
to drive myometrial contractions during farrowing.

3.1.2. Oxytocin
Oxytocin (Ot) is a neuropeptide produced predominately in the hypothalamus and
stored in the posterior lobe of the pituitary gland, but Ot synthesis also occurs in the
decidua [42]. The effects of oxytocin and its mechanisms of action are still being elucidated
despite being extensively studied in humans, making the interpretation of data on Ot
concentrations and the presence of receptors problematic (reviewed by [43]). However,
throughout human pregnancy, the release of Ot is slow and circulating levels are kept low
by the action of oxytocinase, an enzyme produced by the fetal membranes and placenta.
Additionally, myometrial receptivity to oxytocin appears to remain low until the latter
stages of pregnancy [41]. In the pig, oxytocin concentrations begin to rise about 7 h before
the birth of the first piglet (reviewed by [44]). Increased E2 concentration and pressure
on the cervix at the time of parturition induce the pituitary to release large amounts
of Ot in a pulsatile manner, as well as increasing the synthesis of Ot from the decidua.
Additionally, the increased blood concentration of oestradiol likely further stimulates
myometrial contractions. This acts to drive the intense contractions associated with stage 2
of parturition via an autocrine pathway, stimulating production of the prostaglandins that
then also act directly on the myometrium to cause contractions. Additionally, an increased
expression of Ot receptors is seen on the myometrium in response to the switch in the
progesterone: oestrogen ratio and to uterine stretch [45]. It should be noted that probably
due to redundancy, Ot does not seem to be vital for successful parturition, but clearly has
a key role within normal systems [46]. Tangentially, Ot appears to also have a role in the
protection of the fetus from hypoxia during parturition [47].

3.1.3. Prostaglandin F2α and Prostaglandin E2

These two prostaglandins (PGs) appear to be the main members of the large prostaglandin
family that influence parturition. In the pig, where CL are present throughout gestation, a
rise in circulating PF2α, probably derived from the placenta, causes both the expression
of nesting behaviour via the increased secretion of prolactin and luteolysis in the days
immediately preceding parturition [48]. This not only releases a reservoir of relaxin (see
Section 3.1.4) stored in granules within the luteal cells [49], but also leads to a fall in proges-
terone concentrations (see Section 3.1.1) as the main source of this hormone being removed.
The other direct effect of PGF2α is the contraction of myometrial cells. In conjunction with
oestrogen, the resulting pressure on the cervix as the fetuses are pushed through the uterus
leads to the excretion of oxytocin from the posterior lobe of the pituitary (see Section 3.1.2).
Prostaglandin E2 is known to stimulate the maturation of the fetus in preparation for
expulsion in humans [50] and probably pigs. It also has a role in cervical ripening and
increasing the intensity of myometrial contractions during parturition [51]. Importantly,
both may also have a role in the pain of parturition. Administration of PGF2α leads to
acute inflammation via augmentation of arterial dilatation and increased microvascular
permeability, whereas PGE2 sensitises peripheral sensory neurons and central sites within
the spinal cord and the brain [52].

3.1.4. Relaxin
The corpora lutea are stimulated to release a surge of relaxin around 12 h prior to
the onset of parturition [53]. This is stimulated by the preceding increase in PGF2α [54].
The increase in relaxin concentration appears to extend the time of uterine myometrial
quiescence past the observed fall in progesterone, as myometrial contractions do not
commence until both progesterone and relaxin levels fall [55]. This delay in myometrial
activity appears to be the main role of relaxin in the pig, although it also plays a role in
inducing cervical softening and dilatation [56] and coordinating uterine contractions during
farrowing [55].
Animals 2022, 12, 2754 6 of 17

3.1.5. Prolactin
The concentration of prolactin in the blood increases gradually prior to parturition, to
eventually peak at the birth of the first piglet [33]. This hormone, secreted from the anterior
pituitary, has been linked with stimulation of nesting behaviour before parturition by some
authors [57], but not others [58]. It does have a role in stimulating mammary development
in preparation for lactation [59] and milk production postpartum [60].

4. Factors Affecting Parturition

4.1. Uterine Acticity and Contractility
For success at parturition, smooth muscle associated with both myometrial and ab-
dominal contractions must work consistently throughout parturition [61]. In the sow, the
understating of myometrial activity throughout the different stages of parturition is limited
and relies heavily on a handful of accounts [12,62–65]. Electromyography (EMG) of the
uterus before and during parturition indicates three main uterine changes, each occurring
rapidly after one other [12,63]. The first, described as the pre-parturient phase, is a shift
in normal myometrial activity 4–9 h before the first fetal expulsion [63]. Contractions at
this stage regularly persist at a steady amplitude and duration [63]. Myometrial frequency
and intensity increase within the last couple of hours in preparation for the birth of the first
piglet and are accompanied by straining from the sow [63]. The second phase of parturition
signifies an increase in mean contraction intensity and amplitude as the body expels fetuses
as promptly as possible [62]. The third, described as the post-parturient phase, includes
placental birth where contractions persist frequently but at a decreased amplitude [12,63].
Disruption to activity, commonly called uterine inertia, can cause significant risk to
both sow and piglets. Uterine tone is a relatively unexplored factor potentially contributing
to the duration and experience of parturition between parities. In women, parity and asso-
ciated muscle tone of the reproductive tract correlate with parturition success [66]. When
examined using EMG, nulliparous women had higher contractility of the reproductive
tract than multiparous women [66]. In the sow, little is known about the effect of muscle
tone and its association with dystocia occurrence. There is better understanding of this in
the cow, where it is believed hypocalcaemia, hormonal disturbances, infection and genetic
weakness of the smooth muscle play a large part in reproductive muscle contraction at
parturition [61]. Improved understanding of the role that muscle tone plays on success in
parturition of the sow is important for improving protocols for management of farrowing
within the industry.

4.2. Duration of Parturition

The duration of parturition in the sow is one of the factors that varies most markedly
between breeds, individuals and parities. Total parturition time will be strongly dependent
on the litter size, but recommendations of what should be defined as normal for total time
and time per piglet are important due to the direct implications to piglet health and survival
and sow wellbeing.

4.2.1. Overall Parturition

Genetic selection for larger litter sizes has seen parturition duration rise over the
past five decades. Research undertaken 50 years ago describes the experience to last, on
average, 2.53 h, but notes a significant degree of variability (ranging from 56 min to 8 h
55 min) between individual sows [27]. More recently, the average parturition time of the
modern hyperprolific sow has been described as an average of 3.58 h [67]. Between 1966
and 2019, average litter sizes have increased from about 11.5 to 14 piglets [27,68]. A change
in the duration of parturition is expected as sows expel a greater number of piglets. With
the demands that a larger number of fetuses place on physiology, it is no surprise that
estimations of dystocia rates have risen from 0.25% to 5% in the modern hyperprolific
lines of today’s production system [68]. In sows experiencing longer farrowing durations,
abnormal piglet positioning, uterine inertia and obstruction of the vaginal canal are often
Animals 2022, 12, 2754 7 of 17

observed [6]. Langendijk [69] noted a significant increase in piglet mortality when farrowing
duration exceeds 8 h, a 24.6% increase over sows farrowing in 2 h or less. Additionally,
in those that survive prolonged farrowing, extended durations have subsequent effects
on sow health and welfare, reduced appetite, fever, reduced colostrum letdown, and
increased sow removal (i.e., wastage) [68,70]. Poor farrowing can increase the risk of
postpartum dysgalactia syndrome (PPDS), a severe and common illness that presents
in the sow shortly after farrowing, which is associated with an interrupted farrowing,
reduced weaning weights and increased piglet mortality [71]. Reproductive failure due to
dystocia-associated illness such as PPDS is believed to contribute to high turnover rates
(as high as 61% in Australian conditions) [72]. Several cross-farm producer questionnaire
studies found that between 44% and 67% of sow cullings were performed on animals with
a parity of three or less [73–76]. The early culling of sows was attributed to large stillborn
rates, undesirable litter sizes and disease [73]. With sows reaching their peak production
between the third and sixth parities, the undesirable culling of young production animals is
costly to the production chain [73]. Therefore, it is imperative for the success of the porcine
industry and the welfare of both sow and piglets that the parturient process for the modern
sow is thoroughly understood. Particularly, a reasonable farrowing timeframe requires
establishment within the modern industry to permit treatment administration to those
farrowing outside appropriate windows.

4.2.2. Inter-Piglet Interval

Inter-piglet interval is defined as the time between the expulsion of one piglet and
the next [77]. It is generally accepted that most sows will farrow with piglet intervals
of 15–22 min [27,29,78,79]. Piglets born in the latter half of farrowing are observed to
experience longer interval times than those born in the first half of a litter [27,80]. This
could be due to sow exhaustion or reduced contraction intensity as farrowing progresses.
Piglets experiencing a longer birthing interval have an increased risk of morbidities due
to hypoxia leading to death in severe cases [79]. Correspondingly, sows who present with
extended straining without the appearance of a piglet are prone to exhaustion, uterine
infection and potentially death if appropriate intervention does not occur [6].
There is some dissent around when it is appropriate to intervene in cases of an exagger-
ated inter-piglet interval, but it is evident that without treatment, the risk to both sow and
piglet is high. Currently, the advice is to manually intervene if 45 min passes after the birth
of a piglet without the subsequent appearance of the next [6]. However, variation between
individual sows makes defining a gold standard for intervention difficult. Although there
is a notable reduction in stillbirths when manual intervention is undertaken, long-term
effects of potentially unwarranted and often nonsterile techniques are questionable [81].
Further research is required to either validate or improve existing intervention protocols
for enhanced sow and piglet welfare.

4.3. Farrowing Accommodation

Housing type influences the process and outcome of farrowing [82–85]. In the field
of human obstetrics, it has been shown that labour proceeds smoothly and rates of dys-
tocia are reduced when women are encouraged to remain mobile throughout the first
stage [86]. However, most sows in intensive production are confined in housing that re-
stricts movement to reduce piglet fatalities and morbidities by savaging and overlay [83].
The trade-off between sow welfare and piglet safety is a complex one, and sow comfort
during parturition should be one of the factors considered.

4.3.1. Freedom of Movement

The farrowing crate commonly used in modern, intensive production systems limits
sow movement at farrowing, allowing piglets time to escape crushing when a sow lies
down [83]. Although successfully reducing overlays, this housing type has been shown to
prolong farrowing duration and increase stillbirth numbers [84], as well as reducing sow
Animals 2022, 12, 2754 8 of 17

welfare, as measured by circulating cortisol concentration [87]. In contrast, the farrowing

pen provides sows with the ability to move freely, but gives a greater opportunity to injure
piglets [83]. A reduced farrowing duration and inter-piglet interval in sows housed in pens
compared to crated systems has been observed, suggesting a less restricted environment at
parturition has positive effects on progression [26,82,83]. This has a direct impact on the
experience and success of farrowing, as discussed in Section 4.2.
One aspect of research in this area has been in the modification of the housing used
in farrowing to minimise sow confinement without an increase in piglet mortality by
modifying the shape of crates to incorporate anti-crush attachments. Temporary crating
systems (sometimes called free-farrowing systems) allow for sows to be confined for a
shorter duration when the chance of piglet overlay is greater, before the system is converted
into a pen configuration to give greater freedom of movement [88]. When comparing free-
housed sows to sows housed in one of these systems (Sow Welfare and Piglet Protection;
SWAP pens), behavioural differences were minimal, suggesting short-term confinement
could be the happy medium between piglet and sow welfare at parturition [88,89]. There
are moves in some countries towards legislating the use of these pens [90], driven in part by
the “End of the cage age” Citizens’ Initiative in the European Union [90]. Increased scrutiny
of welfare in the pig industry means temporary crating systems could be implemented
globally in the future.

4.3.2. Availability of Nesting Material

The benefits of providing nesting material to sows at farrowing has long been demon-
strated [91]. Like their wild relatives, many domestic sows instinctively perform nest-
building behaviour, including pawing, rooting and seeking nesting material in preparation
for piglet arrival [92]. Such behaviours are believed to support endogenous hormonal
changes at partition, particularly the secretion of oxytocin [84]. When these behaviours are
hindered, the endocrine profile is altered, causing increased stress and, subsequently, re-
duced welfare. As Oliviero et al. [54] reported, sows unable to express natural nest-making
behaviours experience increased circulating cortisol (a biomarker of stress) prior to farrow-
ing and reduced oxytocin secretion during the expulsive period of parturition. Additionally,
Oliviero et al. [84] noted an average 1.5 h increase in the duration of parturition and an
extended inter-piglet interval in sows unable to perform nesting behaviours compared to
those in free housing with access to nesting materials. Plush et al. [93] observed a reduced
incidence of piglet mortality when sows housed in conventional farrowing crates were
provided with foraging materials over those without. Where loose nesting material is not
feasible due to drainage systems, larger materials less susceptible to falling into grates,
such as hessian sacks, may be used. In order to improve both sow and piglet welfare, it is
important to enable the farrowing sow to exhibit some natural behaviours.

4.3.3. Environmental Conditions

For optimal farrowing, the local environment should be free from external stressors.
Increased plasma cortisol concentrations in the sow when ambient temperatures rise above
25 ◦ C warrants careful management within production systems [94]. The evaporative criti-
cal temperature for the sow is 22 ◦ C, and temperatures above this stimulate evaporative
cooling through increased respiration from the lungs [95]. Stress associated with high ambi-
ent temperatures prolongs the farrowing duration and reduces appetite at lactation [95,96].
Elevated relative humidity levels exasperate the effect of high air temperature, making
adaptive cooling difficult for the sow [97]. Hence, the temperature within farrowing sheds
should be monitored closely and maintained below 22 ◦ C with a relative air humidity
between 60–70% to minimise stress and energy usage [95,97].
Moving sows and gilts to farrowing units between days 95–105 of gestation allows for
their habitation to new surroundings and significantly reduces restless behaviour before
parturition compared to the movement of sows at day 114 of gestation [98]. The introduction
to farrowing units too close to parturition can alter maternal behaviour and disrupt the
Animals 2022, 12, 2754 9 of 17

farrowing process, risking the welfare of both sow and piglets [98]. In systems where
temporary crating exists, additional care can minimise stress, particularly in primiparous
animals experiencing the parturient process for the first time. Crating gilts and sows
after parturition has commenced increases farrowing duration [99]. In contrast, confining
animals two days before farrowing inside their loose-housed pens does not affect the
duration of parturition [89].

4.4. Sow Parity

There is some speculation surrounding the effects of sow parity, particularly the differ-
ences between multiparous animals (parities 2+), on the parturient process of the modern
sow. Putting gilts (parity 1) aside, several authors provide evidence to suggest there is no
significant interaction between the parity of a sow and the duration of farrowing [26,29,100].
Contrastingly, others contest this and present evidence to support farrowing duration in-
creasing alongside sow parity [101–104]. Ju et al. [102] suggest this could be due to the
aging of the uterine muscle tissue after multiple farrowings, reducing the ability to contract,
and hence, prolonging the parturient process. It was also shown that factors such as litter
size, body condition and environment are highly correlated with parturition success and
determining the effect of parity alone is difficult [102]. Although the effect of parity is under
debate, it is agreed that the parturient experience is highly variable between animals and,
as such, each case should be observed objectively to ensure both sow and piglet welfare.
Contrastingly, the gilt (parity 1) is perceived as a separate consideration when ex-
amining potential farrowing success. During parturient periods, gilts often present with
enhanced agitation (continuous standing up and lying back down) over higher parity
sows [105]. As a result of increased stress, savaging events are more likely and tend to
occur within the birth of the first two piglets [105]. Early savaging in gilts has been attested
to their lack of familiarity with the birthing process and has been tied to farrowing in a
confined environment [106]. Although the progressive portion of parturition often develops
more promptly in gilts than sows of higher parities, the total duration is similar irrespective
of parity [105]. An early study suggests that stress experienced by gilts at first farrowing
directly correlates with oxytocin secretion, which would otherwise be opioid-mediated,
subsequently enhancing the speed at which the pre-parturient phase progresses [107]. To
ensure success at parturition in the gilt, efforts must be placed on monitoring parturition
progression and reducing any unnecessary additional stressors.

4.5. Sow Nutrition

The dietary intake of a sow influences the progression of farrowing [26,108–111].
Vigilant monitoring of the sow body condition during gestation is necessary to ensure
correct back-fat coverage at farrowing [26]. Sows with body condition scores above 4 (more
than 21 mm back fat) are often reluctant to move during farrowing. Reduced movement at
parturition is linked to increased farrowing times and is speculated to be due to the inability
to contort fetuses within the birthing track [83]. Conversely, sows with too little back-fat
coverage (<16 mm) risk inadequate energy reserves for high-energy bodily processes such
as parturition and lactation [108]. Consequently, sows must be managed appropriately,
ensuring even fat coverage throughout gestation for success at farrowing.
Associated with sow diet, acute constipation increases pain and discomfort at farrow-
ing, leading to extended farrowing times [26]. Constipation within the sow is common
during periods leading up to and during farrowing as the digestive system reduces activity
in preparation for fetal expulsion [109]. However, extensive periods of abnormal defecation
can indicate further issues such as inadequate water intake [109]. This is especially impor-
tant as the sow requires a higher than usual intake of water at this time in preparation for
milk production [112]. Increased solids within the rectal tract can increase the risk of fetal
obstruction, as they create a force against the adjacent birthing canal [109]. Additionally,
prolonged constipation increases the absorption and release of bacterial endotoxins, which
have been linked to postpartum dysgalactia syndrome [110]. To mitigate risks of constipa-
Animals 2022, 12, 2754 10 of 17

tion at farrowing, sows should be offered feed with increased crude fibre (7–10%) during
late pregnancy [111]. Well-informed decision-making and daily observations of digestive
inconsistencies can improve the parturient experience for the sow, increasing the likelihood
of success at farrowing.

4.6. Piglet Factors

Alongside the impact of maternal physiological processes, there is a general consensus
that piglet factors such as size, presentation and number of fetuses can also significantly
impact parturition duration and success.

4.6.1. Piglet Size

Larger piglets take, on average, longer to be expelled than smaller ones [81,113,114].
This is thought to be a result of increased friction between the fetus and the birthing
canal as it move through the pelvic area [114]. However, Rens and Lende [105] found
placental thickness to incur a greater effect on enlarged birthing intervals than the weight
of individual piglets. Smaller piglets in litters with large size variation have also been
observed to have a higher stillbirth probability [81,113–115]. This may be due to the
increased rate of abnormal birthing positions at farrowing in piglets of a smaller size, or
perhaps, reflects a disadvantage due to resource competition with their larger litter mates
in utero. Additional space around small piglets allows easy contortion of limbs and body
parts as cervical contractions push them through the birthing canal. An even spread of
piglet size within a litter may reduce the occurrence of prolonged farrowings [81]. Although
some effort has been undertaken to determine the effect of piglet size on the parturient
experience, its influence on the incidence of dystocia remains unresolved.

4.6.2. Piglet Presentation

Piglet presentation within the birthing canal can affect the parturient experience for
sows and piglets. Presentation can be classed in five ways (Figure 2): (1) The cranial
presentation of piglets involves the forelegs gathered up against the body, with the head
exiting first. Full extension of the fetal body and limbs allows for free movement along the
birthing canal, making cranial presentation the most desirable of fetal positions. (2) The
caudal presentation of piglets appears as hindlegs first, posteriorly extending away from
the body. Piglets born caudally experience raised lactate levels, pH values, exasperated
inter-piglet intervals, and increased quantities of epinephrine within umbilical cord blood
compared with piglets born cranially [29,116,117]. This indicates increased physiological
stress, an undesirable addition to an already challenging experience that is parturition [29].
(3) A breech presentation involves the hindquarters exciting first, with hindlimbs flexed
forward towards the crown of the fetus. (4) A transverse presentation consists of a lateral
positioning of the body with fore- and hindlimbs exiting last. (5) A poll presentation is
characterised as a bent neck with the head pressed against the body and snout facing
towards the cervix.
Most piglets born are delivered in a cranial position (approximately 50%), with caudal
presentation reported the second most frequently [116]. Observed less often within pig
parturition, breech, transverse and poll presentations can incur additional challenges at
fetal expulsion. Breech, transverse and poll presentations of the fetus increase chances of
lodgement within the birthing canal, extending inter-piglet intervals [118]. Considerable
variation within fetal piglet sizes may increase the occurrence of undesirable fetal presen-
tations [81,117]. Ensuring adequate nutrition during parturition for fetal development
and selection for sows with reduced litter variability may lessen the occurrence of issues
associated with undesirable piglet presentation.
Animals 2022, 12, 2754 11 of 17

Figure 2. Anatomical piglet positioning within the birthing canal at parturition: (a) cranial pre-
sentation involving the head exiting first and forelimbs gathered up against the body; (b) caudal
presentation involving hindlegs first, posteriorly extended away from the body; (c) breech position
involving the hindquarters exciting first and hindlegs flexed forward towards the body; (d) transverse
positioning involving a sideways positioning of the body with fore- and hindlimbs exciting last;
(e) poll presentation involving a bent neck with the head pressed against the body and snout facing
towards the cervix.

4.6.3. Litter Size

The selection for increased litter size across the industry has added additional strain
to sow reproductive anatomy and physiology [119]. In a little over five decades, litter size
has grown by an average of 2.5 piglets from 1966 to 2019, with a litter size up to 22 piglets
reported [6,27,120]. Larger litters take a greater length of time to farrow than smaller litters,
directly affecting the occurrence of piglet asphyxiation and sow dystocia. Expelling a
larger number of fetuses can increase the risk of uterine inertia, lodgement of fetuses and
misconfiguration of piglets in the reproductive tract [6]. Additionally, infection or injury
of the reproductive tract due to increased physiological demands of enlarged litter sizes
can affect future sow reproductive performance [66]. To counteract risks associated with
larger litters, monitoring sow wellbeing, inter-piglet intervals and piglet activity levels at
farrowing is advisable [78,79]. Prompt detection and implementation of aid to animals
experiencing prolonged farrowings can improve the welfare of both sows and piglets
undergoing parturition under increased production pressures.
Animals 2022, 12, 2754 12 of 17

5. Induction of Parturition
The preceding information describes the situation in a naturally induced parturition.
It is important to note that in many production systems, it is common to induce farrowing
either for ease of management or veterinary intervention when sows are experiencing an
extended pregnancy. For example, a survey of UK-based pig producers in 2016 demon-
strated that approximately 15% of respondents often induced parturition [121]. Farrowing
induction is commonly performed by the administration of PGF2α or an analogue around
the anticipated due date to initiate luteolysis and, therefore, trigger parturition. However,
the regime of administration varies, with single, double or multiple doses at varying con-
centrations [122]. In some instances, this PGF2α is supplemented with the subsequent
administration of oxytocin or an analogue to stimulate myometrial contractions [123].
The most common reason for induction is because it is desirable to have sows farrow
in standard working hours, to enable more cost-effective supervision. The increased obser-
vation of farrowings improves piglet outcome by reducing stillborn and postnatal mortality
rates [78,124]. This improved outcome from the supervision of farrowing can be offset by a
lower piglet survival rate when sows are induced [78], especially when induction occurs
too early in gestation [122,123], and by increased rates of PPDS in sows [125]. However,
a recent meta-analysis has concluded that under the right conditions, the induction of
parturition in sows with PGF2α or an analogue has no effect on piglet outcome [122] and
may be beneficial in allowing for the greater observation of sows when parturition occurs
in daylight hours.

6. Concluding Remarks
Mammalian parturition is a complex process with many factors influencing the out-
comes, especially in polytocous species such as the pig. Key concepts to consider when
defining “normal” parturition in pigs include parity, litter size, piglet presentation and
farrowing accommodation. These will influence factors such as duration of parturition,
inter-piglet interval and, therefore, overall piglet survival. Other factors not discussed here
that may also be important include overall sow fitness and, perhaps, breed differences. It
is clear that there are gaps in our understanding of the endocrinology and physiology of
this process that should be filled to optimise piglet survival and sow welfare. These gaps
prevent the development of a working definition of dystocia, but the definition will be a
multidimensional one, including, at the least, inter-piglet interval and total duration of
parturition, relative to litter size. Defining this will enable the creation of guidelines to
allow timely and meaningful interventions to occur only when required.

Author Contributions: Writing—original draft preparation, A.W. and R.B.; writing—review and
editing, A.W., R.B., B.H. and S.L.; funding acquisition, R.B. and B.H. All authors have read and agreed
to the published version of the manuscript.
Funding: B.H. was supported by a scholarship from Australian Pork Limited.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the
writing of the manuscript or in the decision to publish.

References
1. Jacobson, C.; Bruce, M.; Kenyon, P.R.; Lockwood, A.; Miller, D.; Refshauge, G.; Masters, D.G. A review of dystocia in sheep. Small
Rumin. 2020, 192, 106209. [CrossRef]
2. Zaborski, D.; Grzesiak, W.; Szatkowska, I.; Dybus, A.; Muszynska, M.; Jedrzejczak, M. Factors affecting dystocia in cattle. Reprod.
Domest. Anim. 2009, 44, 540–551. [CrossRef] [PubMed]
3. Peltoniemi, O.A.T.; Bjorkman, S.; Oliviero, C. Disorders of parturition and the puerperium in the gilt and sow. In Veterinary
Reproduction and Obstetrics, 10th ed.; Noakes, D.E., Parkinson, T.J., England, G.C.W., Eds.; Elsevier: Amsterdam, The Netherlands,
2019; pp. 315–325.
Animals 2022, 12, 2754 13 of 17

4. Andersson, A.; Valros, A.; Rombin, J.; Jensen, P. Extensive infanticide in enclosed European wild boars (Sus scrofa). Appl. Anim.
Behav. Sci. 2011, 134, 184–192. [CrossRef]
5. Harris, M.J.; Bergeron, R.; Gonyou, H.W. Parturient behaviour and offspring-directed aggression in farmed wild boar of three
genetic lines. Appl. Anim. Behav. Sci. 2001, 74, 153–163. [CrossRef]
6. Peltoniemi, O.; Oliviero, C.; Yun, J.; Grahofer, A.; Björkman, S. Management practices to optimize the parturition process in the
hyperprolific sow. J. Anim. Sci. 2020, 98, 96–106. [CrossRef]
7. Kemp, B.; Da Silva, C.L.A.; Soede, N.M. Recent advances in pig reproduction: Focus on impact of genetic selection for female
fertility. Reprod. Domest. Anim. 2018, 53, 28–36. [CrossRef]
8. Kennedy, B.W.; Quinton, V.M.; Smith, C. Genetic changes in Canadian performance-tested pigs for fat depth and growth rate.
Can. J. Anim. Sci. 1995, 76, 41–48.
9. Oliviero, C.; Peltoniemi, O.A.T. Troubled process of parturition of the domestic pig. In Animal Reproduction in Veterinary Medicine;
Aral, F., Ed.; InTech Open: London, UK, 2021; pp. 1–14.
10. Oliviero, C.; Kothe, S.; Heinonen, M.; Valros, A.; Peltoniemi, O.A.T. Prolonged duration of farrowing is associated with subsequent
decresed fertiltiy in sows. Theriogenology 2013, 79, 1095–1099. [CrossRef]
11. Taverne, M.A.M. Physiology of parturition. Anim. Reprod. Sci. 1992, 28, 433–440. [CrossRef]
12. Mainau, E.; Manteca, X. Pain and discomfort caused by parturition in cows and sows. Appl. Anim. Behav. Sci. 2011, 135, 241–251.
[CrossRef]
13. Lally, J.E.; Murtagh, M.M.; Macphail, S.; Thomson, R. More in hope than expectation: A systematic review of women’s expectations
and experience of pain relief in labour. BMC Med. 2008, 6, 7. [CrossRef] [PubMed]
14. Ison, S.H.; Clutton, R.E.; Di Giminiani, P.; Rutherford, K.M.D. A review of pain assessment in pigs. Front. Vet. Sci. 2016, 3, 1–16.
[CrossRef] [PubMed]
15. Ison, S.H.; Jarvis, S.; Rutherford, K.M.D. The identification of potential behavioural indicators of pain in periparturient sows. Res.
Vet. Sci. 2016, 109, 114–120. [CrossRef] [PubMed]
16. Sasaki, Y.; Koketsu, Y. Variability and repeatability in gestation length related to litter performance in female pigs on commercial
farms. Theriogenology 2007, 68, 123–127. [CrossRef]
17. Anderson, L.L. Growth, protein content and distribution of early pig embryos. Anat. Rec. 1978, 190, 143–154. [CrossRef]
18. Leiser, R.; Pfarrer, C.; Abd-Elnaeim, M.; Dantzer, V. Feto-maternal anchorage in epitheliochorial and endotheliochorial placental
types studied by histology and microvascular corrosion casts. Placenta 1998, 12, 21–39. [CrossRef]
19. First, N.L.; Bosc, M.J. Proposed mechanisms controlling parturition and the induction of parturition in swine. J. Anim. Sci. 1979,
48, 1407–1421. [CrossRef]
20. Johansson, R.; Kerestes, D. Quarterly Hogs and Pigs December 2019; USDA-NASS: Washington, DC, USA, 2019.
21. Claxton, G. How Danish pigs are averaging 30 piglets a year. Farmers Weekly. 27 September 2014. Available online:
https://www.fwi.co.uk/livestock/how-danish-sows-are-averaging-30-piglets-a-year (accessed on 2 October 2022).
22. Nam, N.H.; Sukon, P. Non-infectious risk factors for intrapartum stillbirth in a swine farm in the North of Vietnam. Vet. World
2021, 14, 1829–1834. [CrossRef]
23. Cowart, R.P. Parturition and dystocia in swine. In Large Animal Theriogenology; Youngquist, R.S., Threlfall, W.R., Eds.; Elsevier:
Amsterdam, The Netherlands, 2007; pp. 778–784.
24. Alonso-Spilsbury, M.; Mota-Rojas, D.; Martınez-Burnes, J.; Arch, E.; Mayagoitia, A.L.; Ramırez-Necoechea, R.; Olmos, A.;
Trujillo, M.E. Use of oxytocin in penned sows and its effect on fetal intra-partum asphyxia. Anim. Reprod. Sci. 2004, 84, 157–167.
[CrossRef]
25. Zaremba, W.; Udluft, T.; Failing, K.; Bostedt, H. Analysis of the course of birth and the early postpartal period in pigs after
hormonal partus induction with special consideration of complication rate. Anim. Vet. Sci. 2019, 7, 29–39. [CrossRef]
26. Oliviero, C.; Heinonen, M.; Valros, A.; Peltoniemi, O.A.T. Environmental and sow-related factors affecting the duration of
farrowing. Anim. Reprod. Sci. 2010, 119, 85–91. [CrossRef] [PubMed]
27. Jones, J.E.T. Observations on parturition in the sow: Part II: The parturient and post-parturient phases. Br. Vet. J. 1966, 122,
471–478. [CrossRef]
28. Jackson, P.G.G. Chapter 8—Dystocia in the sow. In Handbook of Veterinary Obstetrics, 2nd ed.; Jackson, P.G.G., Ed.; W.B. Saunders:
Oxford, UK, 2004; pp. 129–140.
29. Van Dijk, A.; Van Rens, B.T.T.M.; Van Der Lende, T.; Taverne, M.A.M. Factors affecting duration of the expulsive stage of
parturition and piglet birth intervals in sows with uncomplicated, spontaneous farrowings. Theriogenology 2005, 64, 1573–1590.
[CrossRef] [PubMed]
30. Nam, N.H.; Sukon, P. Risk factors associated with dystocia in swine. Vet. World 2021, 14, 1835–1839. [CrossRef] [PubMed]
31. Liggins, G.C.; Thorburn, G.D. Initiation of parturition. In Marshall’s Physiology of Reproduction, 4th ed.; Lamming, G.E., Ed.;
Springer: Dordrecht, The Netherlands, 1994; Volume 3, pp. 863–1002.
32. Bazer, F.W.; Thatcher, W.W. Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus
exocrine secretion of prostaglandin F2alpha by the uterine endometrium. Prostaglandins 1977, 14, 397–400. [CrossRef]
33. Ellendorff, F.; Taverne, M.; Elsaesser, F.; Forsling, M.; Parvizi, N.; Naaktgeboren, C.; Smidt, D. Endocrinology of parturition in the
pig. Anim. Reprod. Sci. 1979, 2, 323–334. [CrossRef]
Animals 2022, 12, 2754 14 of 17

34. Sherwood, O.D.; Martin, P.A.; Chang, C.C.; Dzuik, P.J. Plasma relaxin levels during late pregnancy and at parturition in pigs with
altered utero-ovarian connections. Biol. Reprod. 1977, 17, 101–103. [CrossRef]
35. Gilbert, C.L. Endocrine regulation of peripartuient behaviour in pigs. Reprod. Suppl. 2001, 58, 263–266.
36. Young, I.R. The comparative physiology of parturition in mammals. Front. Horm. Res. 2001, 27, 10–30. [CrossRef]
37. Van der Meulen, J.; Helmond, F.A.; Oudenaarden, C.P.J. Corpus luteum function in the pig: Progesterone profiles of cyclic and
pregnant gilts. Neth. J. Agri. Sci. 1990, 38, 45–52. [CrossRef]
38. Miller, W.R.; Williams, R.; Pipes, G.W.; Turner, C.W. Conjugation, distribution, and biological half-life (t 1/2) of radioactive
progesterone in plasma and red cells of bovine blood. J. Dairy Sci. 1963, 46, 1402–1404. [CrossRef]
39. Randall, G.C.B.; Tsang, B.K. Influence of the fetal pituitary-adrenal axis on fetal and maternal progesterone and unconjugated
oestrogen concentrations in the pig. J. Reprod. Fertil. 1986, 78, 65–72. [CrossRef] [PubMed]
40. Craig, V.A. Placental steroid metabolism in late pregnancy. In Control of Pig Reproduction; Cole, D.J.A., Foxcroft, G.R., Eds.;
Butterworth Scientific: London, UK, 1982; pp. 405–418.
41. Soloff, M.S.; Swartz, T.L. Characterization of a proposed oxytocin receptor in the uterus of the rat and sow. J. Biol. Chem. 1974,
249, 1376–1381. [CrossRef]
42. Blanks, A.M.; Thorton, S. The role of oxytocin in parturition. BJOG: Int. J. Obstet. Gynaecol. 2003, 110, 46–51. [CrossRef]
43. Carter, C.S.; Kenkel, W.M.; MacLean, E.L.; Wilson, S.R.; Perkeybile, A.M.; Yee, J.R.; Ferris, C.F.; Nazarloo, H.P.; Porges, S.W.;
Davis, J.M.; et al. Is Oxytocin “Nature’s Medicine”? Pharmacol. Rev. 2020, 72, 829–861. [CrossRef]
44. Gilbert, C.L. Oxytocin secretion and management of parturition in the pig. Reprod. Domest. Anim. 1999, 34, 193–200. [CrossRef]
45. Ivell, R.; Kimura, T.; Müller, D.; Augustin, K.; Abend, N.; Bathgate, R.; Telgmann, R.; Balvers, M.; Tillmann, G.; Fuchs, A.-R. The
structure and regulation of the oxytocin receptor. Exp. Physiol. 2001, 86, 289–296. [CrossRef]
46. Russell, J.A.; Leng, G. Sex, parturition and motherhood without oxytocin? J. Endocrinol. 1998, 157, 343–359. [CrossRef]
47. Kingsbury, M.A.; Bilbo, S.D. The inflammatory event of birth: How oxytocin signaling may guide the development of the brain
and gastrointestinal system. Front. Endocrinol. 2019, 55, 100794. [CrossRef]
48. Widowski, T.M.; Curtis, S.E.; Dziuk, P.J.; Wagner, W.C.; Sherwood, O.D. Behavioral and endocrine responses of sows to
prostaglandin F2α and cloprostenol. Biol. Reprod. 1990, 43, 290–297. [CrossRef]
49. Sherwood, O.D. Relaxin’s physiological roles and other diverse actions. Endocr. Rev. 2004, 25, 205–234. [CrossRef] [PubMed]
50. Li, W.-J.; Lu, J.-W.; Zhang, C.-Y.; Wang, W.; Ying, H.; Myatt, L.; Sun, K. PGE2 vs. PGF2α in human parturition. Placenta 2020, 104,
208–219. [CrossRef] [PubMed]
51. Bill, R.; Carmo, L.P.; Vidondo, B.; Nathues, H.; Grahofer, A. Effect of intramuscular and intravaginal PGE-2 treatment compared
to intramuscular oxytocin treatment in eutocic sows on the farrowing performance in a free farrowing system. Theriogenology
2021, 161, 1–7. [CrossRef]
52. Ricciotti, E.; FitzGerald, G.A. Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 986–1000. [CrossRef]
[PubMed]
53. Watts, A.D.; Flint, A.P.F.; Foxcroft, G.R.; Porter, D.G. Plasma steroid, relaxin and dihydro-keto-prostaglandin F2a changes in the
minipig in relation to myometrial electrical and mechanical activity in the prepartum period. J. Reprod. Fertil. 1988, 83, 553–564.
[CrossRef]
54. Sherwood, O.D.; Nara, B.S.; Crnekovic, V.E.; First, N.L. Relaxin concentrations in pig plasma after the administration of
indomethacin and prostaglandin F2a during late pregnancy. Endocrinology 1979, 104, 1716–1721. [CrossRef] [PubMed]
55. Porter, D.G.; Watts, A.D. Relaxin and progesterone are myometrial inhibitors in the ovariectomized non-pregnant mini-pig. J.
Reprod. Fertil. 1986, 76, 205–213. [CrossRef]
56. Kertiles, L.P.; Anderson, L.L. Effect of relaxin on cervical dilatation, parturition and lactiation in the pig. Biol. Reprod. 1979, 21,
57–68. [CrossRef]
57. Castrén, H.; Algers, B.; de Passillé, A.-M.; Rushen, J.; Uvnäs-Moberg, K. Preparturient variation in progesterone, prolactin,
oxytocin and somatostatin in relation to nest building in sows. Appl. Anim. Behav. Sci. 1993, 38, 91–102. [CrossRef]
58. Boulton, M.I.; Wickens, A.; Goode, J.A.; Lawrence, A.B.; Gilbert, C.L. Does Prolactin Mediate Induced Nest-Building Behaviour
inPseudopregnant Gilts Treated with PGF2a? J. Neuroendocrinol. 1998, 10, 601–609. [CrossRef]
59. Farmer, C.; Petitclerc, D. Specific window of prolactin inhibition in late gestation decreases mammary parenchymal tissue
development in gilts. J. Anim. Sci. 2003, 81, 1823–1829. [CrossRef] [PubMed]
60. Smith, B.B.; Wagner, W.C. Effect of dopamine agonists or antagonists, TRH, stress and piglet removal on plasma prolactin
concentrations in lactating gilts. Theriogenology 1985, 23, 283–296. [CrossRef]
61. Simões, J.; Stilwell, G. Dystocia and other abnormal occurrences during calving. In Calving Management and Newborn Calf Care;
Gauly, M., Ed.; Springer International Publishing: Berlin/Heidelberg, Germany, 2021; pp. 81–111.
62. Taverne, M.A.M.; Naaktgeboren, C.; Van Der Weyden, G.C. Myometrial activity and expulsion of fetuses. Anim. Reprod. Sci.
1979, 2, 117–131. [CrossRef]
63. Taverne, M. Myometrial activity during pregnancy and parturition in the pig. In Proceedings-Easter School in Agricultural Science,
University of Nottingham; Nottingham University Press: Nottingham, UK, 1982.
64. Olmos-Hernández, A.; Trujillo-Ortega, M.E.; Alonso-Spilsbury, M.; Sánchez-Aparicio, P.; Ramírez-Necoechea, R.; Mota-Rojas, D.
Foetal Monitoring, Uterine Dynamics and Reproductive Performance in Spontaneous Farrowings in Sows. J. Appl. Anim. Res
2008, 33, 181–185. [CrossRef]
Animals 2022, 12, 2754 15 of 17

65. Taverne, M.A.M.; Naaktgeboren, C.; Elsaesser, F.; Forsling, M.L.; Vanderweyden, G.C.; Ellendorff, F.; Smidt, D. Myometrial
electrical activity and plasma concentrations of progesterone, estrogens and oxytocin during late pregnancy and parturition in
the miniature pig. Biol. Reprod. 1979, 21, 1125–1134. [CrossRef]
66. Petricelli, C.D.; Resende, A.P.M.; Elito Júnior, J.; Araujo Júnior, E.; Alexandre, S.M.; Zanetti, M.R.D.; Nakamura, M.U. Distensibility
and Strength of the Pelvic Floor Muscles of Women in the Third Trimester of Pregnancy. Biomed. Res. Int. 2014, 2014, 1–6.
[CrossRef]
67. Nguyen, N.; Sukon, P. Associated factors for farrowing duration in sows with natural parturition in intensive conditions. J.
World’s Poult. Res. 2020, 10, 320–324. [CrossRef]
68. Oliviero, C.; Junnikkala, S.; Peltoniemi, O. The challenge of large litters on the immune system of the sow and the piglets. Reprod.
Domest. Anim. 2019, 54, 12–21. [CrossRef]
69. Langendijk, P.; Fleuren, M.; Van Hees, H.; Van Kempen, T. The course of parturition affects piglet condition at birth and survival
and growth through the nursery phase. Animals 2018, 8, 60. [CrossRef]
70. Tummaruk, P.; Sang-Gassanee, K. Effect of farrowing duration, parity number and the type of anti-inflammatory drug on
postparturient disorders in sows: A clinical study. Trop. Anim. Health Prod. 2013, 45, 1071–1077. [CrossRef]
71. Heber, L.; Petroman, C.; Petroman, I.; Bălan, I.; Marin, D.; Şandru, O.; Palade, S. Possibilities to Combat MMA Syndrome in Sows.
Sci. Pap. Anim. Sci. Biotech. 2010, 43, 409–411.
72. Hughes, P.; Smits, R.; Xie, Y.; Kirkwood, R. Relationships among gilt and sow live weight, P2 backfat depth, and culling rates. J.
Swine Health Prod. 2010, 18, 301–305.
73. Friendship, R.M.; Wilson, M.R.; Almond, G.W.; McMillan, I.; Hacker, R.R.; Pieper, R.; Swaminathan, S.S. Sow wastage: Reasons
for and effect on productivity. Can. J. Vet. Res. 1986, 50, 205–208. [PubMed]
74. Svendsen, J.; Nielsen, N.C.; Bille, N.; Riising, H.J. Causes of culling and death in sows. Nord Vet. Med. 1975, 27, 604–615.
75. Dagorn, J.; Aumaitre, A. Sow culling: Reasons for and effect on productivity. Livest. Prod. Sci. 1979, 6, 167–177. [CrossRef]
76. Jones, J.E.T. An Investigation of the Causes of Mortality and Morbidity in Sows in a Commercial Herd. Br. Vet. J. 1967, 123,
327–339. [CrossRef]
77. Plush, K.; Weaver, A.; Staveley, L.; Van Wettere, W. Maternal magnesium sulfate supplementation in a pre-farrow diet improves
factors important for piglet viability. Animals 2018, 8, 185. [CrossRef]
78. Holyoake, P.K.; Dial, G.D.; Trigg, T.; King, V.L. Reducing pig mortality through supervision during the perinatal period. J. Anim.
Sci. 1995, 73, 3543–3551. [CrossRef]
79. Okinda, C.; Lu, M.; Nyalala, I.; Li, J.; Shen, M. Asphyxia occurrence detection in sows during the farrowing phase by inter-birth
interval evaluation. Comput. Electron. Agric. 2018, 152, 221–232. [CrossRef]
80. Fraser, D.; Phillips, P.A.; Thompson, B.K. Farrowing behaviour and stillbirth in two environments: An evaluation of the
restraint-stillbirth hypothesis. Appl. Anim. Behav. Sci. 1997, 55, 51–66. [CrossRef]
81. Canario, L.; Cantoni, E.; Le Bihan, E.; Caritez, J.C.; Billon, Y.; Bidanel, J.P.; Foulley, J.L. Between-breed variability of stillbirth and
its relationship with sow and piglet characteristics. J. Anim. Sci. 2006, 84, 3185–3196. [CrossRef] [PubMed]
82. Biensen, N.; Von Borell, E.H.; Ford, S.P. Effects of space allocation and temperature on periparturient maternal behaviors, steroid
concentrations, and piglet growth rates. J. Anim. Sci. 1996, 74, 2641–2648. [CrossRef]
83. Gu, Z.; Gao, Y.; Lin, B.; Zhong, Z.; Liu, Z.; Wang, C.; Li, B. Impacts of a freedom farrowing pen design on sow behaviours
and performancem farrowing pen design on sow behaviours and performance. Prev. Vet. Med. 2011, 102, 296–303. [CrossRef]
[PubMed]
84. Oliviero, C.; Heinonen, M.; Valros, A.; Hälli, O.; Peltoniemi, O.A.T. Effect of the environment on the physiology of the sow during
late pregnancy, farrowing and early lactation. Anim. Reprod. Sci. 2008, 105, 365–377. [CrossRef] [PubMed]
85. Cronin, G.M.; Lefebure, B.; McClintock, S. A comparison of piglet production and survival in the Werribee Farrowing Pen and
conventional farrowing crates at a commercial farm. Aust. J. Exp. Agric. 2000, 40, 17–23. [CrossRef]
86. Lawrence, A.; Lewis, L.; Hofmeyer, G.J.; Styles, C. Maternal positions and mobility during first stage labour (review). Cochrane
Database Syst. Rev. 2013, 10. [CrossRef]
87. Lawrence, A.B.; Petherick, J.C.; McLean, K.A.; Deans, L.A.; Chirnside, J.; Gaughan, A.; Clutton, E.; Terlouw, E.M.C. The effect of
environment on behaviour, plasma cortisol and prolactin in parturient sows. Appl. Anim. Behav. Sci. 1994, 39, 313–330. [CrossRef]
88. Hales, J.; Moustsen, V.A.; Nielsen, M.B.F.; Hansen, C.F. The effect of temporary confinement of hyperprolific sows in Sow Welfare
and Piglet protection pens on sow behaviour and salivary cortisol concentrations. Appl. Anim. Behav. Sci. 2016, 183, 19–27.
[CrossRef]
89. Hansen, C.F.; Hales, J.; Weber, P.M.; Edwards, S.A.; Moustsen, V.A. Confinement of sows 24 h before expected farrowing affects
the performance of nest building behaviours but not progress of parturition. Appl. Anim. Behav. Sci. 2017, 188, 1–8. [CrossRef]
90. 2008/120/EC; Council Directive 2008/120/EC of 18 December 2008 Laying Down Minimum Standards for the Protection of Pigs.
United Nations Environment Programme: Nairobi, Kenya, 2008.
91. Lammers, G.J.; De Lange, A. Pre- and post-farrowing behaviour in primiparous domesticated pigs. Appl. Anim. Behav. Sci. 1986,
15, 31–43. [CrossRef]
92. Gustafsson, M.; Jensen, P.; de Jonge, F.H.; Illmann, G.; Spinka, M. Maternal behaviour of domestic sows and crosses between
domestic sows and wild boar. Appl. Anim. Behav. Sci. 1999, 65, 29–42. [CrossRef]
Animals 2022, 12, 2754 16 of 17

93. Plush, K.J.; McKenny, L.A.; Nowland, T.L.; van Wettere, W.H.E.J. The effect of hessian and straw as nesting materials on sow
behaviour and piglet survival and growth to weaning. Animal 2021, 15, 100273. [CrossRef] [PubMed]
94. Malmkvist, J.; Damgaard, B.M.; Pedersen, L.J.; Jørgensen, E.; Thodberg, K.; Chaloupková, H.; Bruckmaier, R.M. Effects of thermal
environment on hypothalamic-pituitary-adrenal axis hormones, oxytocin, and behavioral activity in periparturient sows. J. Anim.
Sci. 2009, 87, 2796–2805. [CrossRef] [PubMed]
95. Malmkvist, J.; Pedersen, L.J.; Kammersgaard, T.S.; Jørgensen, E. Influence of thermal environment on sows around farrowing and
during the lactation period. J. Anim. Sci. 2012, 90, 3186–3199. [CrossRef] [PubMed]
96. Muns, R.; Malmkvist, J.; Larsen, M.L.V.; Sørensen, D.; Pedersen, L.J. High environmental temperature around farrowing induced
heat stress in crated sows. J. Anim. Sci. 2016, 94, 377–384. [CrossRef] [PubMed]
97. Lucy, M.C.; Safranski, T.J. Heat stress in pregnant sows: Thermal responses and subsequent performance of sows and their
offspring. Mol. Reprod. Dev. 2017, 84, 946–956. [CrossRef]
98. Pedersen, L.J.; Jensen, T. Effects of late introduction of sows to two farrowing environments on the progress of farrowing and
maternal behavior. J. Anim. Sience 2008, 86, 2730–2737. [CrossRef]
99. Yun, J.; Swan, K.-M.; Oliviero, C.; Peltoniemi, O.; Valros, A. Effects of prepartum housing environment on abnormal behaviour,
the farrowing process, and interactions with circulating oxytocin in sows. Appl. Anim. Behav. Sci. 2015, 162, 20–25. [CrossRef]
100. Fahmy, M.H.; Friend, D.W. Factors influencing, and repeatabilty of the duration of farrowing in Yorkshire sows. Can. J. Anim. Sci.
1981, 61, 17–22. [CrossRef]
101. Cronin, G.M.; Schirmer, B.N.; McCallum, T.H.; Smith, J.A.; Butler, K.L. The effects of providing sawdust to pre-parturient sows in
farrowing crates on sow behaviour, the duration of parturition and the occurrence of intra-partum stillborn piglets. Appl. Anim.
Behav. Sci. 1993, 36, 301–315. [CrossRef]
102. Ju, M.; Wang, X.; Li, X.; Zhang, M.; Shi, L.; Hu, P.; Zhang, B.; Han, X.; Wang, K.; Li, X.; et al. Effects of Litter Size and Parity on
Farrowing Duration of Landrace × Yorkshire Sows. Animals 2021, 12, 94. [CrossRef] [PubMed]
103. Lucia, T.; Corrêa, M.N.; Deschamps, J.C.; Bianchi, I.; Donin, M.A.; Machado, A.C.; Meincke, W.; Matheus, J.E.M. Risk factors for
stillbirths in two swine farms in the south of Brazil. Prev. Vet. Med. 2002, 53, 285–292. [CrossRef]
104. Björkman, S.; Oliviero, C.; Rajala-Schultz, P.J.; Soede, N.M.; Peltoniemi, O.A.T. The effect of litter size, parity and farrowing
duration on placenta expulsion and retention in sows. Theriogenology 2017, 92, 36–44. [CrossRef] [PubMed]
105. Rens, B.T.V.; Lende, T.V.D. Parturition in gilts: Duration of farrowing, birth intervals and placenta expulsion in relation to
maternal, piglet and placental traits. Theriogenology 2004, 62, 331–352. [CrossRef] [PubMed]
106. Ahlstrom, S.; Jarvis, S.; Lawrence, A.B. Savaging gilts are more restless and more responsive to piglets during the expulsive phase
of parturition. Appl. Anim. Behav. 2002, 76, 83–91. [CrossRef]
107. Lawrence, A.B.; Petherick, J.C.; McLean, K.A.; Deans, L.; Chirnside, J.; Vaughan, A.; Gilbert, C.L.; Forsling, M.L.; Russell, J.A. The
effects of chronic environmental stress on parturition and on oxytocin and vasopressin secretion in the pig. Anim. Reprod. Sci.
1995, 38, 251–264. [CrossRef]
108. Langendijk, P.; Plush, K. Parturition and its relationship with stillbirths and asphyxiated piglets. Animals 2019, 9, 885. [CrossRef]
109. Pearodwong, P.; Muns, R.; Tummaruk, P. Prevalence of constipation and its influence on post-parturient disorders in tropical
sows. Trop. Anim. Health Prod. 2016, 48, 525–531. [CrossRef]
110. Tabeling, R.; Schwier, S.; Kamphues, J. Effects of different feeding and housing conditions on dry matter content and consistency
of faeces in sows. J. Anim. Physiol. Anim. Nutr. 2003, 87, 116–121. [CrossRef]
111. Oliviero, C.; Kokkonen, T.; Heinonen, M.; Sankari, S.; Peltoniemi, O. Feeding sows with high fibre diet around farrowing and
early lactation: Impact on intestinal activity, energy balance related parameters and litter performance. Res. Vet. Sci. 2009, 86,
314–319. [CrossRef]
112. Mroz, Z.; Jongbloed, A.W.; Lenis, N.P.; Vreman, K. Water in pig nutrition: Physiology, allowances and environmental implications.
Nutr. Res. Rev. 1995, 8, 137–164. [CrossRef] [PubMed]
113. Fahmy, M.H.; Holtmann, W.B.; Macintyre, T.M.; Moxley, J.E. Evaluation of piglet mortality in 28 two-breed crosses among eight
breeds of pig. Anim. Sci. 1978, 26, 277–285. [CrossRef]
114. Motsi, P.; Sakuhuni, C.; Halimani, T.E.; Bhebhe, E.; Ndiweni, P.N.B.; Chimonyo, M. Influence of parity, birth order, litter size and
birth weight on duration of farrowing and birth intervals in commercial exotic sows in Zimbabwe. Anim. Sci. 2006, 82, 569–574.
[CrossRef]
115. Quiniou, N.; Dagorn, J.; Gaudré, D. Variation of piglets’ birth weight and consequences on subsequent performance. Livest. Prod.
Sci. 2002, 78, 63–70. [CrossRef]
116. Herpin, P.; Le Dividich, J.; Hulin, J.C.; Fillaut, M.; De Marco, F.; Bertin, R. Effects of the level of asphyxia during delivery on
viability at birth and early postnatal vitality of newborn pigs. J. Anim. Sci. 1996, 74, 2067–2075. [CrossRef] [PubMed]
117. Mainau, E.; Dalmau, A.; Ruiz-De-La-Torre, J.L.; Manteca, X. A behavioural scale to measure ease of farrowing in sows. Theri-
ogenology 2010, 74, 1279–1287. [CrossRef]
118. Reimers, T.J.; Dziuk, P.J.; Bahr, J.; Sprecher, D.J.; Webel, S.K.; Harmon, B.G. Transuterine embryonal migration in sheep,
anteroposterior orientation of pig and sheep fetuses and presentation of piglets at birth. J. Anim. Sci. 1973, 37, 1212–1217.
[CrossRef]
119. Andersson, E.; Frössling, J.; Engblom, L.; Algers, B.; Gunnarsson, S. Impact of litter size on sow stayability in Swedish commercial
piglet producing herds. Acta Vet. Scand. 2015, 58, 31. [CrossRef]
Animals 2022, 12, 2754 17 of 17

120. Thorsen, C.K.; Schild, S.-L.A.; Rangstrup-Christensen, L.; Bilde, T.; Pedersen, L.J. The effect of farrowing duration on maternal
behavior of hyperprolific sows in organic outdoor production. Livest. Sci. 2017, 204, 92–97. [CrossRef]
121. Ison, S.H.; Jarvis, S.; Rutherford, K.M.D. A survey of sow management at farrowing in the UK. Anim. Welf. 2016, 25, 309–317.
[CrossRef]
122. Monteiro, M.S.; Muro, B.B.D.; Poor, A.P.; Leal, D.F.; Carnevale, R.F.; Shiroma, M.P.; Almond, G.W.; Garbossa, C.A.P.;
Moreno, A.M.; Viana, C.H.C. Effects of farrowing induction with prostaglandins on farrowing traits and piglet performance: A
systematic review and meta-analysis. Theriogenology 2022, 180, 1–16. [CrossRef] [PubMed]
123. Kirkden, R.D.; Broom, D.M.; Andersen, I.L. Piglet mortality: The impact of induction of farrowing using prostaglandins and
oxytocin. Anim. Reprod. Sci. 2013, 138, 14–24. [CrossRef] [PubMed]
124. Mills, K.M.; Shirley, L.K.; Sharp, K.; Garcia, R.; Suarez-Trujillo, A.; Stewart, K.R. Effects of induction on the farrowing process and
piglet blood parameters at the time of farrowing. Transl. Anim. Sci. 2021, 5, txab032. [CrossRef]
125. Papadopoulos, G.A.; Vanderhaeghe, C.; Janssens, G.P.J.; Dewulf, J.; Maes, D.G.D. Risk factors associated with postpartum
dysgalactia syndrome in sows. Vet. J. 2010, 184, 167–171. [CrossRef] [PubMed]